Integration of Vestibular, Visual and Proprioceptive Inputs in the Cerebral Cortex during Movement Control

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The review of the literature data is devoted to the integration of vestibular, visual and proprioceptive inputs in various areas of the cerebral cortex in humans and monkeys during movement control. Despite the abundance of studies of numerous areas of the cortex with vestibular and sensorimotor inputs, their functions and connections are insufficiently studied and understood. The review provides a relatively detailed analysis of data from recent studies of three areas of the cortex involved in motion control: region 7a of the posterior parietal cortex, in which responses to a combined visual-vestibular stimulus tended to dominate the vestibular input over the visual one; the visual region of the cingulate sulcus, which presumably integrates not only visual and vestibular afferent signals, but also proprioceptive signals from the lower limbs, thereby providing interaction between the sensory and motor systems during locomotion; and the area of the superior parietal lobule, in which the visual and somatic inputs interact, allowing you to control behavior when reaching and grasping an object. It is concluded that it is necessary to combine complex natural tasks with normative behavioral models in future research in order to understand how the brain converts sensory input data into a behavioral format.

About the authors

A. M. Badakva

Institute of Biomedical Problems of the RAS

Email: nvmiller@mail.ru
Russia, Moscow

N. V. Miller

Institute of Biomedical Problems of the RAS

Author for correspondence.
Email: nvmiller@mail.ru
Russia, Moscow

L. N. Zobova

Institute of Biomedical Problems of the RAS

Email: nvmiller@mail.ru
Russia, Moscow

References

  1. Feldman A.G., Zhang L. Eye and head movements and vestibulo-ocular reflex in the context of indirect, referent control of motor actions // J. Neurophysiol. 2020. V. 124. № 1. P. 115.
  2. Smith A.T., Greenlee M.W., DeAngelis G.C., Angelaki D.E. Distributed visual–vestibular processing in the cerebral cortex of man and macaque // Multisens. Res. 2017. V. 30. № 2. P. 91.
  3. Chen A., DeAngelis G.C., Angelaki D.E. A comparison of vestibular spatiotemporal tuning in macaque parietoinsular vestibular cortex, ventral intraparietal area, and medial superior temporal area // J. Neurosci. 2011. V. 31. № 8. P. 3082.
  4. Avila E., Lakshminarasimhan K.J., DeAngelis G.C., Angelaki D.E. Visual and vestibular selectivity for self-motion in macaque posterior parietal area 7a // Cerebr. Cortex. 2019. V. 29. № 9. P. 3932.
  5. Smith A.T. Cortical visual area CSv as a cingulate motor area: a sensorimotor interface for the control of locomotion // Brain Struct. Funct. 2021. V. 226. № 9. P. 2931.
  6. Gamberini M., Passarelli L., Filippini M. et al. Vision for action: thalamic and cortical inputs to the macaque superior parietal lobule // Brain Struct. Funct. 2021. V. 226. № 9. P. 2951.
  7. Wilber A.A., Skelin I., Wu W., McNaughton B.L. Laminar organization of encoding and memory reactivation in the parietal cortex // Neuron. 2017. V. 95. № 6. P. 1406.e5.
  8. Kondo H., Saleem K.S., Price J.L. Differential connections of the perirhinal and parahippocampal cortex with the orbital and medial prefrontal networks in macaque monkeys // J. Comp. Neurol. 2005. V. 493. № 4. P. 479.
  9. Barrow C.J., Latto R. The role of inferior parietal cortex and fornix in route following and topograhic orientation in cynomolgus monkeys // Behav. Brain Res. 1996. V. 75. № 1–2. P. 99.
  10. Raffi M., Siegel R.M. A functional architecture of optic flow in the inferior parietal lobule of the behaving monkey // PLoS One. 2007. V. 2. № 2. P. e200.
  11. Pouget A., Sejnowski T.J. Spatial transformations in the parietal cortex using basis functions // J. Cogn. Neurosci. 1997. V. 9. № 2. P. 222.
  12. Rozzi S., Calzavara R., Belmalih A. et al. Cortical connections of the inferior parietal cortical convexity of the macaque monkey // Cereb. Cortex. 2006. V. 16. № 10. P. 1389.
  13. Snyder L.H., Grieve K.L., Brotchie P., Andersen R.A. Separate body-and world-referenced representations of visual space in parietal cortex // Nature. 1998. V. 394. № 6696. P. 887.
  14. Britten K.H. Mechanisms of self-motion perception // Annu. Rev. Neurosci. 2008. V. 31. P. 389.
  15. Chen A., DeAngelis G.C., Angelaki D.E. Functional specializations of the ventral intraparietal area for multisensory heading discrimination // J. Neurosci. 2013. V. 33. № 8. P. 3567.
  16. Medendorp W.P., Heed T. State estimation in posterior parietal cortex: Distinct poles of environmental and bodily states // Prog. Neurobiol. 2019. V. 183. P. 101691.
  17. Dukelow S.P., DeSouza J.F.X., Culham J.C. et al. Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements // J. Neurophysiol. 2001. V. 86. № 4. P. 1991.
  18. Wall M.B., Smith A.T. The representation of egomotion in the human brain // Cur. Biol. 2008. V. 18. № 3. P. 191.
  19. Antal A., Baudewig J., Paulus W., Dechent P. The posterior cingulate cortex and planum temporale/parietal operculum are activated by coherent visual motion // Vis. Neurosci. 2008. V. 25. № 1. P. 17.
  20. Wada A., Sakano Y., Ando H. Differential responses to a visual self-motion signal in human medial cortical regions revealed by wide-view stimulation // Front. Psychol. 2016. V. 7. P. 309.
  21. Pitzalis S., Serra C., Sulpizio V.C. et al. Neural bases of self-and object-motion in a naturalistic vision // Hum. Brain Map. 2020. V. 41. № 4. P. 1084.
  22. Smith A.T., Beer A.L., Furlan M., Mars R.B. Connectivity of the cingulate sulcus visual area (CSv) in the human cerebral cortex // Cereb. Cortex. 2018. V. 28. № 2. P. 713.
  23. Cottereau B.R., Smith A.T., Rima S. et al. Processing of egomotion-consistent optic flow in the rhesus macaque cortex // Cereb. Cortex. 2017. V. 27. № 1. P. 330.
  24. Picard N., Strick P.L. Imaging the premotor areas // Cur. Opin. Neurobiol. 2001. V. 11. № 6. P. 663.
  25. Fetsch C.R., DeAngelis G.C., Angelaki D.E. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons // Nat. Rev. Neurosci. 2013. V. 14. № 6. P. 429.
  26. Habas C. Functional connectivity of the human rostral and caudal cingulate motor areas in the brain resting state at 3T // Neuroradiol. 2010. V. 52. № 1. P. 47.
  27. Serra C., Galletti C., Di Marco S. et al. Egomotion-related visual areas respond to active leg movements // Hum. Brain Map. 2019. V. 40. № 11. P. 3174.
  28. Graziano M.S.A., Cooke D.F., Taylor C.S.R. Coding the location of the arm by sight // Science. 2000. V. 290. № 5497. P. 1782.
  29. Galletti C., Fattori P. The dorsal visual stream revisited: stable circuits or dynamic pathways? // Cortex. 2018. V. 98. P. 203.
  30. Galletti C., Fattori P., Gamberini M., Kutz D.F. The cortical visual area V6: brain location and visual topography // Eur. J. Neurosci. 1999. V. 11. № 11. P. 3922.
  31. Gamberini M., Dal B.G., Breveglieri R. et al. Sensory properties of the caudal aspect of the macaque’s superior parietal lobule // Brain Struct. Funct. 2018. V. 223. № 4. P. 1863.
  32. De Vitis M., Breveglieri R., Hadjidimitrakis K. et al. The neglected medial part of macaque area PE: segregated processing of reach depth and direction // Brain Struct. Funct. 2019. V. 224. № 7. P. 2537.
  33. Galletti C., Fattori P. Neuronal mechanisms for detection of motion in the field of view // Neuropsychologia. 2003. V. 41. № 13. P. 1717.
  34. Gamberini M., Passarelli L., Fattori P., Galletti C. Structural connectivity and functional properties of the macaque superior parietal lobule // Brain Struct. Funct. 2020. V. 225. № 4. P. 1349.
  35. Fattori P., Breveglieri R., Bosco A. et al. Vision for prehension in the medial parietal cortex // Cereb. Cortex. 2017. V. 27. № 2. P. 1149.
  36. Pitzalis S., Hadj-Bouziane F., Dal Bò G. et al. Optic flow selectivity in the macaque parieto-occipital sulcus // Brain Struct. Funct. 2021. V. 226. № 9. P. 2911.
  37. Di Marco S., Fattori P., Galati G. et al. Preference for locomotion-compatible curved paths and forward direction of self-motion in somatomotor and visual areas // Cortex. 2021. V. 137. P. 74.
  38. Hadjidimitrakis K., Bertozzi F., Breveglieri R. et al. Temporal stability of reference frames in monkey area V6A during a reaching task in 3D space // Brain Struct. Funct. 2017. V. 222. № 4. P. 1959.
  39. Diomedi S., Vaccari F.E., Filippini M. et al. Mixed selectivity in macaque medial parietal cortex during eye-hand reaching // iScience. 2020. V. 23. № 10. P. 101616.
  40. Pitzalis S., Serra C., Sulpizio V. et al. A putative human homologue of the macaque area PEc // Neuroimage. 2019. V. 202. P. 116092.
  41. Rathelot J.A., Dum R.P., Strick P.L. Posterior parietal cortex contains a command apparatus for hand movements // Proc. Natl. Acad. Sci. U.S.A. 2017. V. 114. № 16. P. 4255.
  42. Passarelli L., Gamberini M., Fattori P. The superior parietal lobule of primates: A sensory-motor hub for interaction with the environment // J. Integr. Neurosci. 2021. V. 20. № 1. P. 157.
  43. Cullen K.E. Vestibular processing during natural self-motion: implications for perception and action // Nat. Rev. Neurosci. 2019. V. 20. № 6. P. 346.
  44. Lakshminarasimhan K.J., Pouget A., DeAngelis G.C. et al. Inferring decoding strategies for multiple correlated neural populations // PLoS Comput. Biol. 2018. V. 14. № 9. P. e1006371.

Copyright (c) 2023 А.М. Бадаква, Н.В. Миллер, Л.Н. Зобова

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies